Blood Oxygen Depletion Is Independent of Dive Function in a Deep Diving Vertebrate, the Northern Elephant Seal

Abstract

Although energetics is fundamental to animal ecology, traditional methods of determining metabolic rate are neither direct nor instantaneous. Recently, continuous blood oxygen (O2) measurements were used to assess energy expenditure in diving elephant seals (Mirounga angustirostris), demonstrating that an exceptional hypoxemic tolerance and exquisite management of blood O2 stores underlie the extraordinary diving capability of this consummate diver. As the detailed relationship of energy expenditure and dive behavior remains unknown, we integrated behavior, ecology, and physiology to characterize the costs of different types of dives of elephant seals. Elephant seal dive profiles were analyzed and O2 utilization was classified according to dive type (overall function of dive: transit, foraging, food processing/rest). This is the first account linking behavior at this level with in vivo blood O2 measurements in an animal freely diving at sea, allowing us to assess patterns of O2 utilization and energy expenditure between various behaviors and activities in an animal in the wild. In routine dives of elephant seals, the blood O2 store was significantly depleted to a similar range irrespective of dive function, suggesting that all dive types have equal costs in terms of blood O2 depletion. Here, we present the first physiological evidence that all dive types have similarly high blood O2 demands, supporting an energy balance strategy achieved by devoting one major task to a given dive, thereby separating dive functions into distinct dive types. This strategy may optimize O2 store utilization and recovery, consequently maximizing time underwater and allowing these animals to take full advantage of their underwater resources. This approach may be important to optimizing energy expenditure throughout a dive bout or at-sea foraging trip and is well suited to the lifestyle of an elephant seal, which spends > 90% of its time at sea submerged making diving its most “natural” state.

Drift dives and prolonged surfacing periods in Baikal seals: resting strategies in open waters?

“…Our suggestion is supported by the previous finding that blood oxygen stores are depleted to a similar level during diving in elephant seals, irrespective of dive type (i.e. foraging dives and drift dives; Meir et al, 2013).…”

Counting calories in cormorants: dynamic body acceleration predicts daily energy expenditure measured in pelagic cormorants

“…In other diving homeotherms, activity does not correlate well with energy expenditure (Fahlman et al, 2008;Halsey et al, 2011;Meir et al, 2013;Volpov et al, 2015). We argue that in addition to mechanical activity, dive costs are strongly affected by the suppression of oxygen consumption via reduced heart rate, body temperature, shunting of blood past non-vital organs and other mechanisms, and that physiology, in addition to physics, plays an important role in oxygen consumption during dives.…”

“…The same exponential model improves estimation of dive costs in auks (Elliott et al, 2013b). Several authors have observed that activity does not predict energy consumption during diving by homeotherms (Halsey et al, 2011;Meir et al, 2013); one possible explanation for this is that activity costs are overwhelmed by hypometabolism. Evidence for such hypometabolism has been observed in other cormorant species (Bevan et al, 1997).…”

“…Indeed, several studies have failed to find a relationship between DBA and energy expenditure, either when body mass variation may have confounded relationships (Guillemette and Butler, 2012;Dalton et al, 2014;Volpov et al, 2015; M. Kristiansen, Can energy expenditure of free-ranging kittiwakes be estimated by body acceleration? MSc thesis, University of Tromso, 2014) or when cardiovascular adjustments during diving overwhelmed any relationship with mechanical work (Halsey et al, 2011;Meir et al, 2013). It is therefore important to validate DBA in free-living animals, especially across different locomotory modes, temperatures and other vagaries present in the wild environment.…”

Regional variability in diving physiology and behavior in a widely distributed air-breathing marine predator, the South American sea lionOtaria byronia

“…emperor penguins, Aptenodytes forsteri; rhinoceros auklets, Cerorhinca monocerata; Weddell seals, Leptonychotes weddelli; northern elephant seals, Mirounga angustirostris; etc. (Burns, 1999;Hassrick et al, 2013;Meir et al, 2013;Ponganis et al, 2011;Yamamoto et al, 2011)], or on the diving behavior of specific species with restricted distributions [e.g. Australian sea lion, Neophoca cinerea (Fowler et al, 2007); New Zealand sea lion, Phocarctos hookeri (Costa et al, 1998;Leung et al, 2014); Galapagos sea lion, Zalophus wollabaecki (Villegas-Amtmann and ].…”